www.nature.com/scientificreports
SCIENTIFIC REPORTS
OPEN
Received: 18 April 2016 Accepted: 12 July 2016 Published: 16 August 2016
Left extrastriate body area is sensitive to the meaning of symbolic gesture: evidence from fMRI repetition suppression
Agnieszka Kubiak & Gregory Króliczak
Functional magnetic resonance imaging (fMRI) adaptation (a.k.a. repetition suppression) paradigm was used to test if semantic information contained in object-related (transitive) pantomimes and communicative (intransitive) gestures is represented differently in the occipito-temporal cortex. Participants watched 2.75 s back-to-back videos where the meaning of gesture was either repeated or changed. The just observed (typically second) gesture was then imitated. To maintain participants' attention, some trials contained a single video. fMRI adaptation-signal decreases-for watching both movement categories were observed particularly in the lateral occipital cortex, including the extrastriate body area (EBA). Yet, intransitive (vs. transitive) gesture specific repetition suppression was found mainly in the left rostral EBA and caudal middle temporal gyrus- the rEBA/cMTG complex. Repetition enhancement (signal increase) was revealed in the precuneus. While the whole brain and region-of-interest analyses indicate that the precuneus is involved only in visuospatial action processing for later imitation, the common EBA repetition suppression discloses sensitivity to the meaning of symbolic gesture, namely the "semantic what"of actions. Moreover, the rEBA/cMTG suppression reveals greater selectivity for conventionalized communicative gesture.Thus, fMRI adaptation shows higher-orderfunctions of EBA, its role in the semantic network, and indicates that its functional repertoire is wider than previously thought.
Recent behavioral, neuroimaging, and neuropsychological evidencei_4 indicates that performance of meaningful hand movements typically engages a common left-lateralized praxis representation network (PRN)2, regardless of whether these are object- (e.g., tool use/transitive) or non-object-related (intransitive) gestures. Moreover, there is now convincing evidence that the latter category of skilled movements (also referred to as communicative gestures) invokes these same neural resources less than pantomimed tool useu. These conclusions are, never-theless, based almost entirely on research involving simulated actions retrieved from stored representations2,5 or gesture imitation4,6,7. Relatively little is known on whether or not a similar common network would also underlie discrimination or recognition ofboth gesture categories, especially when their processing precedes imitation of the observed movements8_1°. Even if a common network is engaged in watching transitive and intransitive gesture but, besides ditferences in the strength of its engagement, there are locally distinct mechanisms devoted to certain aspects of stimulus processing11,12, it should be possible to identify these disparate functional subdivisions utilizing an fMRI adaptation paradigm13. An example of an adaptation trial used in this study, with its structure and timing is shown in Fig. 1.
fMRI adaptation capitalizes on the repetition suppression (RS) effects14 linked to stimulus-specific decreases in neural activity, as measured by the blood oxygen level dependent (BOLD) signal. RS is typically observed for back-to-back stimuli15, including their characteristic features, and repeated actions directed towards them16, but was also demonstrated for performed back-to-back meaningful gestures17. The mechanisms that may underlie the observed fMRI adaptation effects include the sharpening of the neural response18, its facilitation/accumulation19, or even neural fatigue20. Regardless of the mechanism(s) involved, the paradigms utilizing RS seem to be most
Action and Cognition Laboratory, Institute of Psychology, Department of Social Sciences, Adam Mickiewicz University in Poznań, Poznań, Poland. Correspondence and requests for materials should be addressed to G.K. (email: krolgreg@amu.edu.pl or krol.greg@gmail.com)
SCIENTIFIC REPORTS | 6:31064 | DOI: 10.1038/srep31064 1